Current sampling of genomic sequence data from eukaryotes is relatively poor, biased, and inadequate to address important questions about their biology, evolution, and ecology; this Community Page describes a resource of 700 transcriptomes from marine microbial eukaryotes to help understand their role in the world's oceans.
International audienceCoccolithophores have influenced the global climate for over 200 million years1. These marine phytoplankton can account for 20 per cent of total carbon fixation in some systems2. They form blooms that can occupy hundreds of thousands of square kilometres and are distinguished by their elegantly sculpted calcium carbonate exoskeletons (coccoliths), rendering them visible from space3. Although coccolithophores export carbon in the form of organic matter and calcite to the sea floor, they also release CO2 in the calcification process. Hence, they have a complex influence on the carbon cycle, driving either CO2 production or uptake, sequestration and export to the deep ocean4. Here we report the first haptophyte reference genome, from the coccolithophore Emiliania huxleyi strain CCMP1516, and sequences from 13 additional isolates. Our analyses reveal a pan genome (core genes plus genes distributed variably between strains) probably supported by an atypical complement of repetitive sequence in the genome. Comparisons across strains demonstrate that E. huxleyi, which has long been considered a single species, harbours extensive genome variability reflected in different metabolic repertoires. Genome variability within this species complex seems to underpin its capacity both to thrive in habitats ranging from the equator to the subarctic and to form large-scale episodic blooms under a wide variety of environmental conditions
Many protist plankton are mixotrophs, combining phototrophy and phagotrophy. Their role in freshwater and marine ecology has emerged as a major developing feature of plankton research over recent decades. To better aid discussions, we suggest these organisms are termed “mixoplankton”, as “planktonic protist organisms that express, or have potential to express, phototrophy and phagotrophy”. The term “phytoplankton” then describes phototrophic organisms incapable of phagotrophy. “Protozooplankton” describes phagotrophic protists that do not engage in acquired phototrophy. The complexity of the changes to the conceptual base of the plankton trophic web caused by inclusion of mixoplanktonic activities are such that we suggest that the restructured description is termed the “mixoplankton paradigm”. Implications and opportunities for revision of survey and fieldwork, of laboratory experiments and of simulation modelling are considered. The main challenges are not only with taxonomic and functional identifications, and with measuring rates of potentially competing processes within single cells, but with decades of inertia built around the traditional paradigm that assumes a separation of trophic processes between different organisms. In keeping with the synergistic nature of cooperative photo- and phagotrophy in mixoplankton, a comprehensive multidisciplinary approach will be required to tackle the task ahead.
Transgenerational effects can buffer populations against environmental change, yet little is known about underlying mechanisms, their persistence or the influence of environmental cue timing. We investigated mitochondrial respiratory capacity (MRC) and gene expression of marine sticklebacks that experienced acute or developmental acclimation to simulated ocean warming (21°C) across three generations. Previous work showed that acute acclimation of grandmothers to 21°C led to lower (optimized) offspring MRCs. Here, developmental acclimation of mothers to 21°C led to higher, but more efficient offspring MRCs. Offspring with a 21°C × 17°C grandmother‐mother environment mismatch showed metabolic compensation: their MRCs were as low as offspring with a 17°C thermal history across generations. Transcriptional analyses showed primarily maternal but also grandmaternal environment effects: genes involved in metabolism and mitochondrial protein biosynthesis were differentially expressed when mothers developed at 21°C, whereas 21°C grandmothers influenced genes involved in hemostasis and apoptosis. Genes involved in mitochondrial respiration all showed higher expression when mothers developed at 21° and lower expression in the 21°C × 17°C group, matching the phenotypic pattern for MRCs. Our study links transcriptomics to physiology under climate change, and demonstrates that mechanisms underlying transgenerational effects persist across multiple generations with specific outcomes depending on acclimation type and environmental mismatch between generations.
Global change will affect multiple physico-chemical parameters of the oceans, amongst them also the abundances of macronutrients like phosphorus and nitrogen that are critical for phytoplankton growth. Here, we assessed the transcriptomic responses to phosphorus (P) depletion in the haploid and diploid life-cycle stage of the coccolithophore Emiliania huxleyi (RCC1217/1216) and compared the results with an existing dataset on nitrogen (N) depletion. The responses to the two depletion scenarios within one particular life-cycle stage were more similar at the transcriptome level than the responses of the two stages toward only one particular depletion scenario, emphasizing the tripartite nature of the coccolithophore genome. When cells senesced in both scenarios, they applied functionally similar programs to shut down cell-cycling, readjust biochemical pathways, and increase metabolic turnover to efficiently recycle elements. Those genes that exclusively responded to either P-or N-depletion modulated the general response to enhance scavenging, uptake, and attempted storage of the limiting nutrient. The metabolic adjustments during senescence involved conserved and ancient pathways (e.g., proline oxidation or the glycolytic bypass) that prolong survival on the one hand, but on the other hand give rise to toxic messengers (e.g., reactive oxygen species or methylglyoxal). Continued senescence thus promotes various processes that lead to cell death, which can be delayed only for a limited time. As a consequence, the interplay of the involved processes determines how long cells can endure severe nutrient depletion before they lyse and provide their constituent nutrients to the more viable competitors in their environment. These responses to nutrient depletion are observable in other phytoplankton, but it appears that E. huxleyi's outstanding endurance under nutrient deficiency is due to its versatile high-affinity uptake systems and an efficient, NAD-independent malate oxidation that is absent from most other taxa.
Coccolithophores, especially the abundant, cosmopolitan species Emiliania huxleyi (Lohmann) W. W. Hay et H. P. Mohler, are one of the main driving forces of the oceanic carbonate pump and contribute significantly to global carbon cycling, due to their ability to calcify. A recent study indicates that termination of diploid blooms by viral infection induces life-cycle transition, and speculation has arisen about the role of the haploid, noncalcifying stage in coccolithophore ecology. To explore gene expression patterns in both life-cycle stages, haploid and diploid cells of E. huxleyi (RCC 1217 and RCC 1216) were acclimated to limiting and saturating photon flux densities. Transcriptome analyses were performed to assess differential genomic expression related to different ploidy levels and acclimation light intensities. Analyses indicated that life-cycle stages exhibit different properties of regulating genome expression (e.g., pronounced gene activation and gene silencing in the diploid stage), proteome maintenance (e.g., increased turnover of proteins in the haploid stage), as well as metabolic processing (e.g., pronounced primary metabolism and motility in the haploid stage and calcification in the diploid stage). Furthermore, higher abundances of transcripts related to endocytotic and digestive machinery were observed in the diploid stage. A qualitative feeding experiment indicated that both life-cycle stages are capable of particle uptake (0.5 lm diameter) in late-stationary growth phase. Results showed that the two life-cycle stages represent functionally distinct entities that are evolutionarily shaped to thrive in the environment they typically inhabit.
The globally occurring Alexandrium tamarense/fundyense/catenella species complex consists of toxic and non-toxic strains that are morphologically difficult to distinguish. We developed four specific ribosomal RNA probes that can identify the entire species complex, the strains of the toxic North American clade and the strains of the two non-toxic clades from Western Europe and the Mediterranean Sea by DNA dot blot and fluorescence in situ hybridization. These probes are a first step for the development of an early warning system for the presence of A. tamarense.
Intraspecific trait diversity can promote the success of a species, as complementarity of functional traits within populations may enhance its competitive success and facilitates resilience to changing environmental conditions. Here, we experimentally determined the variation and relationships between traits in 15 strains of the toxic dinoflagellate Alexandrium ostenfeldii derived from two populations. Measured traits included growth rate, cell size, elemental composition, nitrogen uptake kinetics, toxin production and allelochemical potency. Our results demonstrate substantial variation in all analysed traits both within and across populations, particularly in nitrogen affinity, which was even comparable to interspecific variation across phytoplankton species. We found distinct trade-offs between maximum nitrogen uptake rate and affinity, and between defensive and competitive traits. Furthermore, we identified differences in trait variation between the genetically similar populations. The observed high trait variation may facilitate development and resilience of harmful algal blooms under dynamic environmental conditions.
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